Donor Fecal Microbiota Transplantation Alters Gut Microbiota and Metabolites in Obese Individuals With Steatohepatitis
The intestinal microbiota has been linked to the development and prevalence of steatohepatitis in humans. Interestingly, steatohepatitis is significantly lower in individuals taking a plant‐based, low‐animal‐protein diet, which is thought to be mediated by gut microbiota. However, data on causality...
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| Published in | Hepatology communications Vol. 4; no. 11; pp. 1578 - 1590 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Wolters Kluwer Health Medical Research, Lippincott Williams & Wilkins
01.11.2020
John Wiley and Sons Inc Wolters Kluwer Health/LWW |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The intestinal microbiota has been linked to the development and prevalence of steatohepatitis in humans. Interestingly, steatohepatitis is significantly lower in individuals taking a plant‐based, low‐animal‐protein diet, which is thought to be mediated by gut microbiota. However, data on causality between these observations in humans is scarce. In this regard, fecal microbiota transplantation (FMT) using healthy donors is safe and is capable of changing microbial composition in human disease. We therefore performed a double‐blind randomized controlled proof‐of‐principle study in which individuals with hepatic steatosis on ultrasound were randomized to two study arms: lean vegan donor (allogenic n = 10) or own (autologous n = 11) FMT. Both were performed three times at 8‐week intervals. A liver biopsy was performed at baseline and after 24 weeks in every subject to determine histopathology (Nonalcoholic Steatohepatitis Clinical Research Network) classification and changes in hepatic gene expression based on RNA sequencing. Secondary outcome parameters were changes in intestinal microbiota composition and fasting plasma metabolomics. We observed a trend toward improved necro‐inflammatory histology, and found significant changes in expression of hepatic genes involved in inflammation and lipid metabolism following allogenic FMT. Intestinal microbial community structure changed following allogenic FMT, which was associated with changes in plasma metabolites as well as markers of . Conclusion: Allogenic FMT using lean vegan donors in individuals with hepatic steatosis shows an effect on intestinal microbiota composition, which is associated with beneficial changes in plasma metabolites and markers of steatohepatitis. |
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| AbstractList | The intestinal microbiota has been linked to the development and prevalence of steatohepatitis in humans. Interestingly, steatohepatitis is significantly lower in individuals taking a plant-based, low-animal-protein diet, which is thought to be mediated by gut microbiota. However, data on causality between these observations in humans is scarce. In this regard, fecal microbiota transplantation (FMT) using healthy donors is safe and is capable of changing microbial composition in human disease. We therefore performed a double-blind randomized controlled proof-of-principle study in which individuals with hepatic steatosis on ultrasound were randomized to two study arms: lean vegan donor (allogenic n = 10) or own (autologous n = 11) FMT. Both were performed three times at 8-week intervals. A liver biopsy was performed at baseline and after 24 weeks in every subject to determine histopathology (Nonalcoholic Steatohepatitis Clinical Research Network) classification and changes in hepatic gene expression based on RNA sequencing. Secondary outcome parameters were changes in intestinal microbiota composition and fasting plasma metabolomics. We observed a trend toward improved necro-inflammatory histology, and found significant changes in expression of hepatic genes involved in inflammation and lipid metabolism following allogenic FMT. Intestinal microbial community structure changed following allogenic FMT, which was associated with changes in plasma metabolites as well as markers of . Conclusion: Allogenic FMT using lean vegan donors in individuals with hepatic steatosis shows an effect on intestinal microbiota composition, which is associated with beneficial changes in plasma metabolites and markers of steatohepatitis.The intestinal microbiota has been linked to the development and prevalence of steatohepatitis in humans. Interestingly, steatohepatitis is significantly lower in individuals taking a plant-based, low-animal-protein diet, which is thought to be mediated by gut microbiota. However, data on causality between these observations in humans is scarce. In this regard, fecal microbiota transplantation (FMT) using healthy donors is safe and is capable of changing microbial composition in human disease. We therefore performed a double-blind randomized controlled proof-of-principle study in which individuals with hepatic steatosis on ultrasound were randomized to two study arms: lean vegan donor (allogenic n = 10) or own (autologous n = 11) FMT. Both were performed three times at 8-week intervals. A liver biopsy was performed at baseline and after 24 weeks in every subject to determine histopathology (Nonalcoholic Steatohepatitis Clinical Research Network) classification and changes in hepatic gene expression based on RNA sequencing. Secondary outcome parameters were changes in intestinal microbiota composition and fasting plasma metabolomics. We observed a trend toward improved necro-inflammatory histology, and found significant changes in expression of hepatic genes involved in inflammation and lipid metabolism following allogenic FMT. Intestinal microbial community structure changed following allogenic FMT, which was associated with changes in plasma metabolites as well as markers of . Conclusion: Allogenic FMT using lean vegan donors in individuals with hepatic steatosis shows an effect on intestinal microbiota composition, which is associated with beneficial changes in plasma metabolites and markers of steatohepatitis. The intestinal microbiota has been linked to the development and prevalence of steatohepatitis in humans. Interestingly, steatohepatitis is significantly lower in individuals taking a plant-based, low-animal-protein diet, which is thought to be mediated by gut microbiota. However, data on causality between these observations in humans is scarce. In this regard, fecal microbiota transplantation (FMT) using healthy donors is safe and is capable of changing microbial composition in human disease. We therefore performed a double-blind randomized controlled proof-of-principle study in which individuals with hepatic steatosis on ultrasound were randomized to two study arms: lean vegan donor (allogenic n = 10) or own (autologous n = 11) FMT. Both were performed three times at 8-week intervals. A liver biopsy was performed at baseline and after 24 weeks in every subject to determine histopathology (Nonalcoholic Steatohepatitis Clinical Research Network) classification and changes in hepatic gene expression based on RNA sequencing. Secondary outcome parameters were changes in intestinal microbiota composition and fasting plasma metabolomics. We observed a trend toward improved necro-inflammatory histology, and found significant changes in expression of hepatic genes involved in inflammation and lipid metabolism following allogenic FMT. Intestinal microbial community structure changed following allogenic FMT, which was associated with changes in plasma metabolites as well as markers of . Allogenic FMT using lean vegan donors in individuals with hepatic steatosis shows an effect on intestinal microbiota composition, which is associated with beneficial changes in plasma metabolites and markers of steatohepatitis. The intestinal microbiota has been linked to the development and prevalence of steatohepatitis in humans. Interestingly, steatohepatitis is significantly lower in individuals taking a plant‐based, low‐animal‐protein diet, which is thought to be mediated by gut microbiota. However, data on causality between these observations in humans is scarce. In this regard, fecal microbiota transplantation (FMT) using healthy donors is safe and is capable of changing microbial composition in human disease. We therefore performed a double‐blind randomized controlled proof‐of‐principle study in which individuals with hepatic steatosis on ultrasound were randomized to two study arms: lean vegan donor (allogenic n = 10) or own (autologous n = 11) FMT. Both were performed three times at 8‐week intervals. A liver biopsy was performed at baseline and after 24 weeks in every subject to determine histopathology (Nonalcoholic Steatohepatitis Clinical Research Network) classification and changes in hepatic gene expression based on RNA sequencing. Secondary outcome parameters were changes in intestinal microbiota composition and fasting plasma metabolomics. We observed a trend toward improved necro‐inflammatory histology, and found significant changes in expression of hepatic genes involved in inflammation and lipid metabolism following allogenic FMT. Intestinal microbial community structure changed following allogenic FMT, which was associated with changes in plasma metabolites as well as markers of . Conclusion: Allogenic FMT using lean vegan donors in individuals with hepatic steatosis shows an effect on intestinal microbiota composition, which is associated with beneficial changes in plasma metabolites and markers of steatohepatitis. The intestinal microbiota has been linked to the development and prevalence of steatohepatitis in humans. Interestingly, steatohepatitis is significantly lower in individuals taking a plant‐based, low‐animal‐protein diet, which is thought to be mediated by gut microbiota. However, data on causality between these observations in humans is scarce. In this regard, fecal microbiota transplantation (FMT) using healthy donors is safe and is capable of changing microbial composition in human disease. We therefore performed a double‐blind randomized controlled proof‐of‐principle study in which individuals with hepatic steatosis on ultrasound were randomized to two study arms: lean vegan donor (allogenic n = 10) or own (autologous n = 11) FMT. Both were performed three times at 8‐week intervals. A liver biopsy was performed at baseline and after 24 weeks in every subject to determine histopathology (Nonalcoholic Steatohepatitis Clinical Research Network) classification and changes in hepatic gene expression based on RNA sequencing. Secondary outcome parameters were changes in intestinal microbiota composition and fasting plasma metabolomics. We observed a trend toward improved necro‐inflammatory histology, and found significant changes in expression of hepatic genes involved in inflammation and lipid metabolism following allogenic FMT. Intestinal microbial community structure changed following allogenic FMT, which was associated with changes in plasma metabolites as well as markers of . Conclusion: Allogenic FMT using lean vegan donors in individuals with hepatic steatosis shows an effect on intestinal microbiota composition, which is associated with beneficial changes in plasma metabolites and markers of steatohepatitis. The intestinal microbiota has been linked to the development and prevalence of steatohepatitis in humans. Interestingly, steatohepatitis is significantly lower in individuals taking a plant‐based, low‐animal‐protein diet, which is thought to be mediated by gut microbiota. However, data on causality between these observations in humans is scarce. In this regard, fecal microbiota transplantation (FMT) using healthy donors is safe and is capable of changing microbial composition in human disease. We therefore performed a double‐blind randomized controlled proof‐of‐principle study in which individuals with hepatic steatosis on ultrasound were randomized to two study arms: lean vegan donor (allogenic n = 10) or own (autologous n = 11) FMT. Both were performed three times at 8‐week intervals. A liver biopsy was performed at baseline and after 24 weeks in every subject to determine histopathology (Nonalcoholic Steatohepatitis Clinical Research Network) classification and changes in hepatic gene expression based on RNA sequencing. Secondary outcome parameters were changes in intestinal microbiota composition and fasting plasma metabolomics. We observed a trend toward improved necro‐inflammatory histology, and found significant changes in expression of hepatic genes involved in inflammation and lipid metabolism following allogenic FMT. Intestinal microbial community structure changed following allogenic FMT, which was associated with changes in plasma metabolites as well as markers of . Conclusion: Allogenic FMT using lean vegan donors in individuals with hepatic steatosis shows an effect on intestinal microbiota composition, which is associated with beneficial changes in plasma metabolites and markers of steatohepatitis. |
| Author | Meijnikman, Abraham S. Aron‐Wisnewky, Judith Holleboom, Adriaan G. Zoetendal, Erwin G. Bergman, Jacques J. Lienden, Krijn Winkelmeijer, Maaike Runge, Jurgen H. Nieuwdorp, Max Witjes, Julia J. Levin, Evgeni Vos, Willem Smits, Loek P. Bouter, Kristien E.C. Verheij, Joanne Mannisto, Ville Prodan, Andrei Herrema, Hilde Pekmez, Ceyda T. Nederveen, Aart J. Troelstra, Marian A. Beuers, Ulrich H. Konstanti, Prokopis Groen, Albert K. Dragsted, Lars O. |
| AuthorAffiliation | 1 Department of Internal and Vascular Medicine Amsterdam University Medical Centers Location AMC Amsterdam the Netherlands 5 Laboratory of Microbiology Wageningen University Wageningen the Netherlands 2 Department of Nutrition, Exercise and Sports University of Copenhagen Copenhagen Denmark 4 Department of Gastroenterology and Hepatology Amsterdam University Medical Centers Location AMC Amsterdam the Netherlands 3 Department of Radiology & Nuclear Medicine Amsterdam University Medical Centers Location AMC Amsterdam the Netherlands 7 Department of Pathology Amsterdam University Medical Centers Location AMC Amsterdam the Netherlands 8 Department of Laboratory Medicine University of Groningen University Medical Center Groningen the Netherlands 6 Faculty of Medicine Human Microbiome Research Program University of Helsinki Finland |
| AuthorAffiliation_xml | – name: 8 Department of Laboratory Medicine University of Groningen University Medical Center Groningen the Netherlands – name: 1 Department of Internal and Vascular Medicine Amsterdam University Medical Centers Location AMC Amsterdam the Netherlands – name: 6 Faculty of Medicine Human Microbiome Research Program University of Helsinki Finland – name: 7 Department of Pathology Amsterdam University Medical Centers Location AMC Amsterdam the Netherlands – name: 3 Department of Radiology & Nuclear Medicine Amsterdam University Medical Centers Location AMC Amsterdam the Netherlands – name: 2 Department of Nutrition, Exercise and Sports University of Copenhagen Copenhagen Denmark – name: 4 Department of Gastroenterology and Hepatology Amsterdam University Medical Centers Location AMC Amsterdam the Netherlands – name: 5 Laboratory of Microbiology Wageningen University Wageningen the Netherlands |
| Author_xml | – sequence: 1 givenname: Julia J. surname: Witjes fullname: Witjes, Julia J. organization: Location AMC – sequence: 2 givenname: Loek P. surname: Smits fullname: Smits, Loek P. organization: Location AMC – sequence: 3 givenname: Ceyda T. surname: Pekmez fullname: Pekmez, Ceyda T. organization: University of Copenhagen – sequence: 4 givenname: Andrei surname: Prodan fullname: Prodan, Andrei organization: Location AMC – sequence: 5 givenname: Abraham S. surname: Meijnikman fullname: Meijnikman, Abraham S. organization: Location AMC – sequence: 6 givenname: Marian A. surname: Troelstra fullname: Troelstra, Marian A. organization: Location AMC – sequence: 7 givenname: Kristien E.C. surname: Bouter fullname: Bouter, Kristien E.C. organization: Location AMC – sequence: 8 givenname: Hilde surname: Herrema fullname: Herrema, Hilde organization: Location AMC – sequence: 9 givenname: Evgeni surname: Levin fullname: Levin, Evgeni organization: Location AMC – sequence: 10 givenname: Adriaan G. surname: Holleboom fullname: Holleboom, Adriaan G. organization: Location AMC – sequence: 11 givenname: Maaike surname: Winkelmeijer fullname: Winkelmeijer, Maaike organization: Location AMC – sequence: 12 givenname: Ulrich H. surname: Beuers fullname: Beuers, Ulrich H. organization: Location AMC – sequence: 13 givenname: Krijn surname: Lienden fullname: Lienden, Krijn organization: Location AMC – sequence: 14 givenname: Judith surname: Aron‐Wisnewky fullname: Aron‐Wisnewky, Judith organization: Location AMC – sequence: 15 givenname: Ville surname: Mannisto fullname: Mannisto, Ville organization: Location AMC – sequence: 16 givenname: Jacques J. surname: Bergman fullname: Bergman, Jacques J. organization: Location AMC – sequence: 17 givenname: Jurgen H. surname: Runge fullname: Runge, Jurgen H. organization: Location AMC – sequence: 18 givenname: Aart J. surname: Nederveen fullname: Nederveen, Aart J. organization: Location AMC – sequence: 19 givenname: Lars O. surname: Dragsted fullname: Dragsted, Lars O. organization: University of Copenhagen – sequence: 20 givenname: Prokopis surname: Konstanti fullname: Konstanti, Prokopis organization: Wageningen University – sequence: 21 givenname: Erwin G. surname: Zoetendal fullname: Zoetendal, Erwin G. organization: Wageningen University – sequence: 22 givenname: Willem surname: Vos fullname: Vos, Willem organization: University of Helsinki – sequence: 23 givenname: Joanne surname: Verheij fullname: Verheij, Joanne organization: Location AMC – sequence: 24 givenname: Albert K. surname: Groen fullname: Groen, Albert K. organization: University Medical Center – sequence: 25 givenname: Max surname: Nieuwdorp fullname: Nieuwdorp, Max email: m.nieuwdorp@amsterdamumc.nl organization: Location AMC |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33163830$$D View this record in MEDLINE/PubMed |
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| Copyright | 2020 The Authors. Hepatology Communications published by Wiley Periodicals LLC on behalf of the American Association for the Study of Liver Diseases. 2020. This work is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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| License | Attribution-NonCommercial-NoDerivs http://creativecommons.org/licenses/by-nc-nd/4.0 2020 The Authors. Hepatology Communications published by Wiley Periodicals LLC on behalf of the American Association for the Study of Liver Diseases. This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made. |
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| Notes | These authors contributed equally to this work. Supported by Hartstichting (Grant/Award No. 2012‐03) and Fondation Leducq (Grant/Award No. 17CVD01). Clinical Trial Registration – Trial NL4189 (NTR4339). Potential conflict of interest: Dr. Aron‐Wisnewsky received grants from the Bettencourt Schueller Foundation. Dr. Nieuwdorp and Dr. de Vos own stock in, consult for, and has intellectual property rights in Caelus Health. He consults for Kaleido. None of these are directly relevant to the current paper. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 ObjectType-Review-3 content type line 23 |
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| References | 2017; 2 2018; 129 2003; 114 2017; 357 2016; 34 2018; 7 2020; 6 2018; 39 2013; 59 2014; 5 2017; 70 2005; 268 2019; 69 2014; 15 2016; 310 2019; 157 2005; 37 2010; 72 2019; 8 2012; 143 2019; 70 2015; 4 2019; 30 2019; 2 2020; 180 2017; 67 2019; 38 2005; 41 2007; 91 2006; 1 2010; 81 2010; 40 2018; 24 2006; 355 2018; 68 2016; 6 2015; 62 2015; 61 2020 2018; 555 2015; 21 2016; 65 2016; 63 2012; 718 2009; 9 2020; 69 2016; 535 2018; 51 2009; 6 (hep41601-bib-0037-20240114) 2019; 70 (hep41601-bib-0036-20240114) 2019; 8 (hep41601-bib-0012-20240114) 2016; 65 (hep41601-bib-0029-20240114) 2010; 72 (hep41601-bib-0008-20240114) 2019; 30 (hep41601-bib-0010-20240114) 2016; 63 (hep41601-bib-0038-20240114) 2016; 310 (hep41601-bib-0035-20240114) 2020 (hep41601-bib-0028-20240114) 2006; 355 (hep41601-bib-0017-20240114) 2012; 143 (hep41601-bib-0019-20240114) 2018; 7 (hep41601-bib-0022-20240114) 2015; 4 (hep41601-bib-0044-20240114) 2007; 91 (hep41601-bib-0004-20240114) 2015; 61 (hep41601-bib-0003-20240114) 2015; 62 (hep41601-bib-0040-20240114) 2017; 2 (hep41601-bib-0021-20240114) 2016; 34 (hep41601-bib-0025-20240114) 2017; 70 (hep41601-bib-0011-20240114) 2019; 38 (hep41601-bib-0015-20240114) 2018; 39 (hep41601-bib-0042-20240114) 2016; 535 (hep41601-bib-0048-20240114) 2009; 9 (hep41601-bib-0001-20240114) 2019; 69 (hep41601-bib-0013-20240114) 2018; 129 (hep41601-bib-0027-20240114) 2006; 1 (hep41601-bib-0050-20240114) 2018; 555 (hep41601-bib-0005-20240114) 2017; 67 (hep41601-bib-0006-20240114) 2019; 2 (hep41601-bib-0043-20240114) 2019; 157 (hep41601-bib-0023-20240114) 2014; 15 (hep41601-bib-0046-20240114) 2020; 6 (hep41601-bib-0020-20240114) 2005; 41 (hep41601-bib-0024-20240114) 2012; 718 (hep41601-bib-0031-20240114) 2015; 21 (hep41601-bib-0033-20240114) 2018; 51 (hep41601-bib-0039-20240114) 2017; 357 (hep41601-bib-0007-20240114) 2016; 65 (hep41601-bib-0045-20240114) 2018; 68 (hep41601-bib-0032-20240114) 2010; 40 (hep41601-bib-0030-20240114) 2005; 268 (hep41601-bib-0034-20240114) 2009; 6 (hep41601-bib-0049-20240114) 2003; 114 (hep41601-bib-0002-20240114) 2013; 59 (hep41601-bib-0026-20240114) 2010; 81 (hep41601-bib-0016-20240114) 2020; 180 (hep41601-bib-0047-20240114) 2014; 5 (hep41601-bib-0018-20240114) 2020; 69 (hep41601-bib-0041-20240114) 2005; 37 (hep41601-bib-0009-20240114) 2018; 24 (hep41601-bib-0014-20240114) 2016; 6 |
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| SubjectTerms | Biopsy Body mass index Diabetes Diet Fatty liver Feces Gastrointestinal surgery Gene expression Gut microbiota Hepatitis Inflammation Liver diseases Metabolic syndrome Metabolites Microbiota Original Plasma Proteins Ultrasonic imaging Veganism Vegetarianism |
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| Title | Donor Fecal Microbiota Transplantation Alters Gut Microbiota and Metabolites in Obese Individuals With Steatohepatitis |
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